José C. Noguera

Oxidative stress and life histories: unresolved issues and current needs

Abstract Life‐history theory concerns the trade‐offs that mold the patterns of investment by animals between reproduction, growth, and survival. It is widely recognized that physiology plays a role in the mediation of life‐history trade‐offs, but the details remain obscure. As life‐history theory concerns aspects of investment in the soma that influence survival, understanding the physiological basis of life histories is related, but not identical, to understanding the process of aging. One idea from the field of aging that has gained considerable traction in the area of life histories is that life‐history trade‐offs may be mediated by free radical production and oxidative stress. We outline here developments in this field and summarize a number of important unresolved issues that may guide future research efforts. The issues are as follows. First, different tissues and macromolecular targets of oxidative stress respond differently during reproduction. The functional significance of these changes, however, remains uncertain. Consequently there is a need for studies that link oxidative stress measurements to functional outcomes, such as survival. Second, measurements of oxidative stress are often highly invasive or terminal. Terminal studies of oxidative stress in wild animals, where detailed life‐history information is available, cannot generally be performed without compromising the aims of the studies that generated the life‐history data. There is a need therefore for novel non‐invasive measurements of multi‐tissue oxidative stress. Third, laboratory studies provide unrivaled opportunities for experimental manipulation but may fail to expose the physiology underpinning life‐history effects, because of the benign laboratory environment. Fourth, the idea that oxidative stress might underlie life‐history trade‐offs does not make specific enough predictions that are amenable to testing. Moreover, there is a paucity of good alternative theoretical models on which contrasting predictions might be based. Fifth, there is an enormous diversity of life‐history variation to test the idea that oxidative stress may be a key mediator. So far we have only scratched the surface. Broadening the scope may reveal new strategies linked to the processes of oxidative damage and repair. Finally, understanding the trade‐offs in life histories and understanding the process of aging are related but not identical questions. Scientists inhabiting these two spheres of activity seldom collide, yet they have much to learn from each other.

Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird

Exposure to stressors early in life is associated with faster ageing and reduced longevity. One important mechanism that could underlie these late life effects is increased telomere loss. Telomere length in early post-natal life is an important predictor of subsequent lifespan, but the factors underpinning its variability are poorly understood. Recent human studies have linked stress exposure to increased telomere loss. These studies have of necessity been non-experimental and are consequently subjected to several confounding factors; also, being based on leucocyte populations, where cell composition is variable and some telomere restoration can occur, the extent to which these effects extend beyond the immune system has been questioned. In this study, we experimentally manipulated stress exposure early in post-natal life in nestling European shags (Phalacrocorax aristotelis) in the wild and examined the effect on telomere length in erythrocytes. Our results show that greater stress exposure during early post-natal life increases telomere loss at this life-history stage, and that such an effect is not confined to immune cells. The delayed effects of increased telomere attrition in early life could therefore give rise to a ‘time bomb’ that reduces longevity in the absence of any obvious phenotypic consequences early in life.

Pre-fledgling oxidative damage predicts recruitment in a long-lived bird

Empirical evidence has shown that stressful conditions experienced during development may exert long-term negative effects on life-history traits. Although it has been suggested that oxidative stress has long-term effects, little is known about delayed consequences of oxidative stress experienced early in life in fitness-related traits. Here, we tested whether oxidative stress during development has long-term effects on a life-history trait directly related to fitness in three colonies of European shags Phalacrocorax aristotelis. Our results revealed that recruitment probability decreased with oxidative damage during the nestling period; oxidative damage, in turn, was related to the level of antioxidant capacity. Our results suggest a link between oxidative stress during development and survival to adulthood, a key element of population dynamics.

Heritability of resistance to oxidative stress in early life

Oxidative stress has recently been suggested to play an important role in life‐history evolution, but little is known about natural variation and heritability of this physiological trait. Here, we explore phenotypic variation in resistance to oxidative stress of cross‐fostered yellow‐legged gull (Larus cachinnans) chicks. Resistance to oxidative stress was not related to plasma antioxidants at hatching, which are mostly derived from maternal investment into eggs. Common environmental effects on phenotypic variation in resistance to oxidative stress were not significant. Heritability was relatively low and nonsignificant in hatchlings, but interestingly, the chicks of age 8 days showed high and significant heritability (h2 = 0.59). Our results suggest that resistance to oxidative stress is determined mainly by the genotype as chicks grow. Further work is required to explore the genetic role of oxidative stress in life‐history evolution.

Sex-dependent effects of nutrition on telomere dynamics in zebra finches (Taeniopygia guttata)

At a cellular level, oxidative stress is known to increase telomere attrition, and hence cellular senescence and risk of disease. It has been proposed that dietary micronutrients play an important role in telomere protection due to their antioxidant properties. We experimentally manipulated dietary micronutrients during early life in zebra finches (Taeniopygia guttata). We found no effects of micronutrient intake on telomere loss during chick growth. However, females given a diet high in micronutrients during sexual maturation showed reduced telomere loss; there was no such effect in males. These results suggest that micronutrients may influence rates of cellular senescence, but differences in micronutrient requirement and allocation strategies, probably linked to the development of sexual coloration, may underlie sex differences in response.

Senescent males carry premutagenic lesions in sperm

As organisms age, DNA of somatic cells deteriorates, but it is believed that germ cells are protected from DNA‐damaging agents. In recent years, this vision has been challenged by studies on humans indicating that genomic instability in germ cells increases with age. However, nothing is known about germ line senescence in wild animals. Here, we examine DNA damage in sperm of a wild vertebrate, the blue‐footed booby Sula nebouxii. One of the major types of premutagenic DNA damage generated by oxidative stress (a proximal cause of ageing) is loss of single bases resulting in apurinic/apyrimidinic sites (AP sites). We examined AP sites in the sperm of known‐age males sampled during courtship on Isla Isabel, Mexico. We show that damage to the DNA of sperm increases with age of male blue‐footed boobies. Moreover, we found that sexual attractiveness (foot colour) declines with age and is correlated with germ line damage of senescent males. By choosing attractive males, females might reduce the probability of their progeny bearing damaged DNA. This study reports the first evidence of senescence in the germ line of a wild vertebrate and future studies should investigate whether this burden of senescence is sidestepped by potential sexual partners.

Vitamins, stress and growth: the availability of antioxidants in early life influences the expression of cryptic genetic variation

Environmental inputs during early development can shape the expression of phenotypes, which has long‐lasting consequences in physiology and life history of an organism. Here, we study whether experimentally manipulated availability of dietary antioxidants, vitamins C and E, influences the expression of genetic variance for antioxidant defence, endocrine signal and body mass in yellow‐legged gull chicks using quantitative genetic models based on full siblings. Our experimental study in a natural population reveals that the expression of genetic variance in total antioxidant capacity in plasma increased in chicks supplemented with vitamins C and E despite the negligible effects on the average phenotype. This suggests that individuals differ in their ability to capture and transport dietary antioxidants or to respond to these extra resources, and importantly, this ability has a genetic basis. Corticosterone level in plasma and body mass were negatively correlated at the phenotypic level. Significant genetic variance of corticosterone level appeared only in control chicks nonsupplemented with vitamins, suggesting that the genetic variation of endocrine system, which transmits environmental cues to adaptively control chick development, appeared in stressful conditions (i.e. poor antioxidant availability). Therefore, environmental inputs may shape evolutionary trajectories of antioxidant capacity and endocrine system by affecting the expression of cryptic genetic variation.

Interactive effects of early and later nutritional conditions on the adult antioxidant defence system in zebra finches

ABSTRACT In vertebrates, antioxidant defences comprise a mixture of endogenously produced components and exogenously obtained antioxidants that are derived mostly from the diet. It has been suggested that early-life micronutritional conditions might influence the way in which the antioxidant defence system operates, which could enable individuals to adjust the activity of the endogenous and exogenous components in line with their expected intake of dietary antioxidants if the future environment resembles the past. We investigated this possibility by experimentally manipulating the micronutrient content of the diet during different periods of postnatal development in the zebra finch (Taeniopygia guttata). Birds that had a low micronutrient diet during the growth phase initially had a lower total antioxidant capacity (TAC) than those reared under a high micronutrient diet, but then showed a compensatory response, so that by the end of the growth phase, the TAC of the two groups was the same. Interestingly, we found an interactive effect of micronutrient intake early and late in development: only those birds that continued with the same dietary treatment (low or high) throughout development showed a significant increase in their TAC during the period of sexual maturation. A similar effect was also found in the level of enzymatic antioxidant defences (glutathione peroxidase; GPx). No significant effects were found in the level of oxidative damage in lipids [malondialdehyde (MDA) levels]. These findings demonstrate the importance of early and late developmental conditions in shaping multiple aspects of the antioxidant system. Furthermore, they suggest that young birds may adjust their antioxidant defences to enable them to ‘thrive’ on diets rich or poor in micronutrients later in life. Summary: Experimentally manipulating the intake of dietary antioxidants in young zebra finches shows that early-life nutrition can shape later-life antioxidant defences.

Are you what you eat? Micronutritional deficiencies during development influence adult personality-related traits

Stressful environmental conditions such as periods of poor nutrition have been shown to affect a variety of life history traits. Although nutrition-induced effects on the phenotype can appear through the entire life of an individual, it is becoming evident that there are sensitive periods during development when phenotypic traits have heightened sensitivity to nutritional conditions. Very few studies have investigated how nutrition can affect an important aspect of an organisms phenotype: the development of its ‘personality’. In this study we manipulated the availability of the main micronutrients (i.e. vitamins and essential minerals) present in the diet of zebra finches, Taeniopygia guttata, during their postnatal development and/or during their sexual maturation. Later, once the birds were fully adult, we assessed a series of behavioural traits previously used to assess personality in birds. We found that low availability of dietary micronutrients during the postnatal period resulted in reduced boldness in males once they reached adulthood, but had no effect on adult stress responses or neophobic behaviour. No such effects were found in females. In contrast, a low micronutrient diet during sexual maturation led in both sexes to reduced stress responses and neophobic behaviours in adulthood. Interestingly, we also found that females became more aggressive as adults if they had received a low micronutrient diet during development, irrespective of when the availability of micronutrients was modified. Overall, our results demonstrate substantial effects of diet on the development of behavioural traits, and that these effects differ both between the sexes and over different developmental periods.

Embryonic and postnatal telomere length decrease with ovulation order within clutches

Telomere length (TL) in early life has been found to be predictive of subsequent lifespan. Factors such as parental TL, parental age and environmental conditions during development have been shown to contribute to the observed variation in TL among individuals. One factor that has not hitherto been considered is ovulation order, although it is well established that the last hatched/born offspring in a brood or litter often show relatively poor subsequent performance. We examined the within- and across-clutch effect of ovulation order on TL in embryos of zebra finches experiencing the same controlled incubation conditions (N = 151), and tested whether any such ovulation order effects remained detectable in adults (N = 122). Irrespective of clutch and egg size, TL in early-stage embryos (72 h incubation) markedly decreased with within-clutch ovulation order; the difference in TL of first and last-laid embryos was equivalent to the average within-individual telomere loss over the entire period of nestling and juvenile life. This ovulation-order effect occurred only within but not across clutches, and was still evident in adults. Given that TL in early life predicts lifespan, our results suggest that parental effects on telomere length could contribute to the known poor performance of later-ovulated family members.